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Flexible Omnivory in Dikerogammarus Villosus (Sowinsky, 1894) (Amphipoda) — Amphipod Pilot Species Project (Ampis) Report 5

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Flexible Omnivory in Dikerogammarus Villosus (Sowinsky, 1894) (Amphipoda) — Amphipod Pilot Species Project (Ampis) Report 5 FLEXIBLE OMNIVORY IN DIKEROGAMMARUS VILLOSUS (SOWINSKY, 1894) (AMPHIPODA) — AMPHIPOD PILOT SPECIES PROJECT (AMPIS) REPORT 5 BY DIRK PLATVOET1,6), GERARD VAN DER VELDE2,3), JAIMIE T. A. DICK4) and SHUQIANG LI5) 1) Zoological Museum, University of Amsterdam, Mauritskade 57, NL-1092 AD Amsterdam, The Netherlands 2) Department of Animal Ecology and Ecophysiology, Institute for Water and Wetland Research, Radboud University Nijmegen, Heijendaalseweg 135, NL-6525 AJ Nijmegen, The Netherlands 3) National Museum of Natural History Naturalis, P.O. Box 9517, NL-2300 RA Leiden, The Netherlands 4) School of Biological Sciences, Medical and Biological Centre, Queen’s University of Belfast, 97 Lisburn Road, Belfast BT9 7BL, Northern Ireland, U.K. 5) Department of Invertebrate Zoology, Institute of Zoology, Chinese Academy of Sciences, Du-Tun Road, Beijing 100101, P.R. China ABSTRACT Feeding in Dikerogammarus villosus (Sowinsky, 1894) males was observed in the field and recorded on video in the laboratory. The following feeding modes were recognized: detritus feeding, grazing, particle feeding, coprophagy, predation on benthic and free swimming invertebrates, predation on fish eggs and larvae, as well as feeding on byssus threads of the zebra mussel, Dreissena polymorpha (Pallas, 1771). The feeding methods are described and illustrated with screenshots of video recordings. The very flexible feeding modes of D. villosus, which make diet switches possible, form a trait that must be an important factor in the invasion success of this Ponto-Caspian gammaridean species, and may thus explain for a great deal its high ecosystem impact. RÉSUMÉ L’alimentation des mâles de Dikerogammarus villosus (Sowinsky, 1894) a été observée dans la nature et enregistrée par vidéo au laboratoire. Les différents modes d’alimentation suivants ont été reconnus: détritivore, broutage, particulaire, coprophage, prédation sur des invertébrés benthiques et nageurs, prédation d’œufs et de larves de poissons, et aussi alimentation sur les amas de la moule rayée Dreissena polymorpha (Pallas, 1771). Les méthodes d’alimentation sont décrites et illustrées avec des photos provenant d’enregistre- ments vidéos. Le mode d’alimentation très flexible de D. villosus, qui permet des changements de 6) e-mail: [email protected] © Koninklijke Brill NV, Leiden, 2009 Crustaceana 82 (6): 703-720 Also available online: www.brill.nl/cr DOI:10.1163/156854009X423201 704 DIRK PLATVOET ET AL. régime, est un trait qui est peut-être un facteur important dans le succès d’invasion de cette espèce de gammaridé Ponto-Caspien et qui peut expliquer en grande partie son fort impact sur l’écosystème. INTRODUCTION Gammaridean amphipods have long been considered purely as shredders of organic material. In a growing number of publications, however, the role of these amphipods in food-webs is put in a different perspective by Gledhill et al. (1993) and Monakov (2003, and literature therein). In Irish river systems, 95% of the macroinvertebrate biomass can consist of Gammarus p. pulex (Linnaeus, 1758), an invasive alien species in Ireland (MacNeil et al., 2000). Assuming that the absence of other macroinvertebrates in these rivers is the result of interaction with this species, then a predatory role of this species becomes rational. Intraguild predation has been recognized as a common phenomenon in gammarideans (Dick et al., 1993). Stable isotope data of Dikerogammarus villosus (Sowinsky, 1894) from the river Rhine indicated that this invasive Ponto-Caspian gammaridean clustered with zoobenthivorous fish in contrast to Gammarus tigrinus Sexton, 1939, which species occurred on a lower trophic level (Marguillier, 1998; Marguillier et al., 1998; Van der Velde et al., 2000; Van Riel et al., 2006b). The appearance of D. villosus in the river Rhine coincided with the decrease of the North American gammaridean, G. tigrinus as well as of other macroinvertebrates, in particular on the stones of groynes and river banks (Van der Velde et al., 2000, 2002; Van Riel et al., 2006a, b). In a Rhine-fed lake in the Netherlands, the IJsselmeer, the appearance of D. villosus coincided with the total disappearance of the native G. duebenii Lilljeborg, 1852 from the stony banks, its only habitat in the lake, whereas G. tigrinus disappeared also from these stones but maintained its population in deeper water in the sediment, and in zebra mussel beds (Platvoet, 2007). Predation on a wide range of other invertebrates was first demonstrated by laboratory experiments (Dick et al., 2002), in which Dikerogammarus villosus proved to be a formidable predator, preying even on predaceous, hard skinned insects such as water bugs and damselfly larvae. However, in the absence of prey, this species is easily able to switch to particle feeding (Platvoet et al., 2006). Being a food generalist is an important characteristic for an invading species (Van der Velde et al., 2000). To determine how flexible D. villosus is with respect to feeding, we studied its feeding-related activities. We also discuss the position of this species, and of gammaridean species in general, in the classification of species as belonging to various feeding guilds or categories. FLEXIBLE OMNIVORY DIKEROGAMMARUS VILLOSUS — AMPIS 5 705 MATERIAL AND METHODS In May 2001, male specimens of Dikerogammarus villosus were collected from Lake Gouwzee, a Rhine-fed, slightly brackish lake that is part of the Markermeer/IJsselmeer complex. The specimens were immediately transferred to the laboratory and stored in a large tank with site water at site temperature (16◦C). Four male specimens of D. villosus were involved in the observations (body length 21-22 mm). In gammaridean amphipods with a pre-copula stage, males are much larger than females. Therefore, males are far more active food collectors than females. Recording on video was done with a JVC digital video camcorder GR-DVL100 on mini DV at the highest resolution. Two types of cuvettes were used: the first experiments were performed with two bolted-together plexi-glass plates separated by a plastic hose bent in U-shape, leaving a 9 mm space between the plates with 25 ml of source water, and later a cuvette was developed consisting of a U-shaped plexi-glass plate of 10 by 10 cm of 9 mm thickness lined with two 2 mm thick glass plates of 10 10 cm, with 16 ml of source water. Both cuvettes were aerated × with a syringe needle connected to a hose and an air pump. Water temperature in the cuvettes was maintained at 19◦C during the experiments, the temperture of the climate room. The males were individually filmed in a total of 20 recording sessions of one hour each. In four one-hour experiments, a mix of several food items was offered to give D. villosus a choice. Most invertebrates offered were collected from a small inland water body where D. villosus is absent, the Oosterpoel bordering the Gouwzee, with equal salinity and temperature as the lake. Water fleas (Daphnia sp.) were obtained from an aquarium shop. A pondweed (Potamogeton pectinatus L.) was collected from Lake Gouwzee. In some experiments, the animals were given an abundant supply of vegetation or invertebrate specimens, in others only a single prey. Generally, potential prey or plants were already present in the cuvette for 15 minutes, before a male D. villosus was added. The males of D. villosus were not starved before the experiments. Coarse sand and gravel served as a substrate in most recordings. Observations were purely qualitative. RESULTS In all experiments a response to the food provided was recorded. It became clear that the abundance of food led to a continuous feeding activity, only interrupted by regular cleaning sessions at intervals of, on average, ten minutes. These cleaning sessions are described below in the particle feeding section. 706 DIRK PLATVOET ET AL. During detritus feeding, grazing, and some forms of predation the individuals actively browsed the substrate, while during predation of free-swimming animals attacks were made from a steady position, like from an ambush (sit and wait strategy). We identified the following feeding-related activities: 1. detritus feeding 2. coprophagy 3. grazing 4. particle feeding 5. predation of free-swimming animals 6. predation on benthic animals 7. predation on fish eggs 8. feeding on byssus threads of zebra mussels 1. Detritus feeding In four experiments, four different males were given a choice of decaying and non-decaying parts (ratio 50/50) of pondweed (Potamogeton pectinatus). Only feeding on decaying parts was observed, and the non-decaying parts were ignored. The first contact with the plant material was made by the first antennae carefully touching it. In a quick response, the second antennae pulled the food towards the outstretched first and second gnathopods. With additional support from the antennae, the food was brought in line with the mouthparts. Finally, the incisors of the mandibles cut off parts that were then moved to the molars for grinding. Fluids and particles were directed towards the oesophagus through a combined action of the inner rami of the maxilliped, the first maxillae, and of both rami of the second maxillae. The feathered setae that line these parts assisted in maintaining a directed flow. 2. Coprophagy The process of re-digestion of faeces in D. villosus started with bringing the urosome towards the mouthparts (fig. 1A–D). The third uropods were always in a horizontal position, ventral side up. The faeces were forced from the rectum in a quick action, lasting between two and four seconds, and then received by either the mouthparts directly or by the third uropods, after which the gnathopods led the faeces to the mouthparts. The inside setae of the inner rami of the third uropods are lined with long, feathered setae, forming a network. The mouthparts apparently manipulated the faeces in such a way that digestible and indigestible fractions were separated, resulting in a cloud of rejected material.
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